The impact of neonatal low level PCB exposure on behavioral performance by monkeys. Studies by Deborah Rice and Stephen Hayward.

These three papers used experimental methodology from operant conditioning (behavioral psychology) to explore low level impacts of postnatal PCB exposure in monkeys (Macaca fascicularis). The studies provide strong evidence that "exposure to an environmentally relevant level of a PCB mixture for a short time postnatally results in long-lasting behavioral effects."

Young monkeys were dosed from birth to 20 weeks of age with 7.5 µg/kg/day of a PCB mixture representative of that typically found in human milk. Three to five years after exposure, their performance on behavioral tests was compared with a control group of monkeys.

Blood PCB levels at the age of 20 weeks were 0.30-0.37 ppb for the controls and 1.84-2.84 ppb for the treated monkeys. PCB levels in the fat were 50-198 ppb and 1694-3560 ppb, respectively. The treated group's contamination level in fat is within the middle of the range of exposures noted for people, whereas the blood level levels in the treated monkey group are at the low end of values seen in people.

Rice has stated at scientific meetings that when the data for exposure levels of the treated monkeys were first given to her, they were mis-reported as being much higher than the levels actually found, and that had she known how low these exposures really were, she probably would not have conducted the experiments. That makes her results even more striking.

Rice, DC. 1998. Effects of postnatal exposure of monkeys to a PCB mixture on spatial discrimination reversal and DRL performance. Neurotoxicology and Teratology 20(4):391-400.

This set of tests was performed 4.5 to 5 years after exposure. Rice found no difference between treated and control group monkeys in a "spatial discrimination reversal" test. In this test, the monkeys were challenged to respond adaptively to changes in the rules they needed to follow to obtain a reward. Part of this test also involved showing the monkeys cues that were irrelevant to solving the task, and seeing if these irrelevant cues increased the error rates. Rice notes that even though there were no differences between the groups, "there was an indication of poorer performance in some treated individuals."

Rice did, however, find significant differences between treated and controls in a "differential reinforcement of low rate" test. In essence, this test measured the ability of the monkeys to be patient. Treated monkeys were much more likely to commit errors in this test, i.e., to be less patient. Rice observed that the control group monkeys in this test clearly "progressively adapted" to the test procedures, whereas the treated group did not.

Rice, DC. 1997. Effects of postnatal exposure to a PCB mixture in monkeys on multiple fixed interval-fixed ratio performance. Neurotoxicology and Teratology 19:1-6.

Rice reports that the exposed monkeys perform differently, compared to controls, in basic behavioral tests. The tests she used were classic approaches used by behavioral psychologists called "fixed ratio" and "fixed interval" "schedules of reinforcement." In these tests the monkeys were given reward of a squirt of apple juice for meeting certain test criteria that were based on pushing a button a certain number of times (fixed ratio) and pushing a button once after a time interval had passed (fixed interval), a "waiting period." In Rice's tests, she mixed these two schedules of reinforcement in a standard way called a "multiple fixed interval (FI)-fixed ratio (FR)" schedule of reinforcement.

Treated monkeys responded to the tests differently compared to control monkeys. The most interesting difference was the treated monkey's response to the "fixed interval" part of the test. Typically, animals and people develop a classic pattern of response to FI tests in which during training they begin to pause after receiving the reward, with the length of the pause over time getting close to the end of the waiting period. Tested at 4 years of age, the treated monkeys developed the pause much more slowly than the experimental monkeys. Even at the end of the experiment, the treated group continued to show a high number of short pauses. "If anything, this difference appeared to be getting larger as the experiment progressed, as control monkeys decreased their short IRTs across sessions and treated monkeys did not. While behavioral psychologists balk at describing this is simpler terms, in essence it is as if the treated monkeys showed much less patience than the control monkeys."

Rice, DC and S Hayward 1997. Effects of postnatal exposure to a PCB mixture in Monkeys on Nonspatial Discrimination Reversal and Delayed Alternation Performance. Neurotoxicology 18:479-494.

These experiments were performed 3 years after exposure. The authors state in conclusion that their "results suggest that postnatal exposure to PCBs produces cognitive deficits in monkeys."

Rice and Hayward took the monkeys through two behavioral tests: a "nonspatial discrimination reversal" (NSR) and a "spatial delayed alternation" (SDA). These are standard tests in operant conditioning.

In essence, the NSR test examines the subject's ability to respond adaptively to changes in the rules that link behavior to reinforcement. The experimenter periodically reverses the rules so that what had been reinforced before no longer is, and vice-versa. Of interest is the quickness with which the subject learns that the rules have changed and the number of errors committed while adapting to the new rules.

The SDA test involved requiring the monkeys to switch the behavior adaptively and introducing delays into the test when errors were committed. More errors then prolonged the delay, i.e., the length of time the monkey had to wait before becoming eligible for another reinforcment.

On the NSR test, Rice and Hayward found some differences between treated and controls but many similarities. They observe; "If there is a relationship between tissue levels of PCBs and performance [on this test] it is a complex one."

In contrast, the treated and control monkeys demonstrated some strong differences on the SDA test. Treated monkeys required significantly more sessions to "reach criterion on the acquisition" [i.e. to perform well enough to "pass" the test]. The treated monkeys made more errors and perservered more in counterproductive behaviors.

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